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Characterization of Aliivibrio Fischeri Strains Associated with Disease Outbreak in Brill Scophthalmus Rhombus

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Characterization of Aliivibrio Fischeri Strains Associated with Disease Outbreak in Brill Scophthalmus Rhombus Vol. 124: 215–222, 2017 DISEASES OF AQUATIC ORGANISMS Published May 11 https://doi.org/10.3354/dao03123 Dis Aquat Org Characterization of Aliivibrio fischeri strains associated with disease outbreak in brill Scophthalmus rhombus Jose R. López*, Laura Lorenzo, Rafael Alcantara, J. I. Navas IFAPA Centro Agua del Pino, Junta de Andalucía, Carretera El Rompido-Punta Umbría km 3.8, CP21450 Cartaya, Huelva, Spain ABSTRACT: Three bacterial isolates were recovered from a disease outbreak with high mortality affecting brill Scophthalmus rhombus (Linnaeus, 1758). Moribund fish showed no external signs of disease, but plentiful haemorrhages were observed in liver. On the basis of phenotypic and genotypic characterization, the isolates were identified as Aliivibrio fischeri. The phenotypic pro- file of the isolates was basically similar to that of the type strain of this species, although some dis- crepancies were observed, mainly in the BIOLOG GN profile. The main cellular fatty acids of strain a591 were also consistent with this species. The highest 16S rDNA sequence similarities were recorded with the type strain of A. fischeri (99.07%); other Aliivibrio species showed similar- ity values below 96%. The highest sequence similarities with gyrB, rpoD and recA genes were also recorded with A. fischeri type strain (99.31, 98.99 and 95.29% similarity, respectively). DNA−DNA hybridization assays confirmed that these isolates belong to A. fischeri; levels of DNA relatedness were 73.5 to 86.2% with isolate a591 (reciprocal values of 86.9 to 99.04%). Finally, a virulence evaluation of the isolates using Senegalese sole fry was also performed; significant mortalities (100% mortality within 5 d) were recorded by intraperitoneal injection, but only with high doses of bacteria (2 × 106 cfu g−1 body weight). KEY WORDS: Fish pathogen · Diagnosis · Identification · Virulence Resale or republication not permitted without written consent of the publisher INTRODUCTION Ruby et al. 2005). These attributes make A. fischeri a useful model organism for examination of microbial The genus Aliivibrio (Gammaproteobacteria: Vibrio - bioluminescence, quorum sensing and bacterial− naceae) was created by Urbanczyk et al. (2007) after animal symbiosis (Dunn 2012). However, A. fischeri reclassification of a number of Vibrio species from the strains have also been found associated with disease former Vibrio fischeri clade, based on phylogenetic outbreaks in shrimp Penaeus monodon (Fabricius, and phenotypic differences. At present, the genus 1798) (Lavilla-Pitogo et al. 1998) and in marine fish in comprises 6 species: A. fischeri, A. logei, A. salmoni- Spain—namely in sea bream Sparus aurata Lin- cida, A. wodanis, A. finisterrensis and A. sifiae. naeus, 1758 and turbot Scophthalmus maximus Lin- A. fischeri, the type species of the genus, can be naeus, 1758 cultures — although its pathogenicity is found either free living in the marine environment or not clear (Lamas et al. 1990, Balebona et al. 1998, associated with a eukaryotic host; in fact, certain bio- Buller 2004). luminescent strains are symbiont in the light-emit- To our knowledge, the present paper reports the ting organs of certain squids and fishes (Farmer 2006, first description and characterization of A. fischeri *Corresponding author: [email protected] © Inter-Research 2017 · www.int-res.com 216 Dis Aquat Org 124: 215–222, 2017 strains associated with a disease outbreak in brill using the MIDI operating system and the aerobic Scophthalmus rhombus. bacteria library TSBA6 (MIDI 2008). MATERIALS AND METHODS Phylogenetic analysis Bacterial isolation Template DNA from pure cultures was prepared by boiling bacterial colonies for 5 min in distilled Mortalities occurred in adult-sized fish (1.7 to water followed by centrifugation at 16 168 × g for 2.8 kg) stocked at 3.5 kg m−2 in a recirculating system 2 min to sediment the cell debris. The concentration with fiberglass tanks. Samples for bacterial isolation and purity of genomic DNA was calculated from were taken from liver and kidney of moribund fish, measurements of absorbance at 260 (A260) and and cultured on Flexibacter maritimus medium 280 nm (A280), recorded using a NanoDrop 1000 (FMM) (Pazos et al. 1996) at 20°C for 24 to 96 h. For spectro photometer. Partial 16S rRNA gene se - long-term preservation, strains were frozen at −80°C quences were obtained using the universal primers in sterile seawater supplemented with 20% (v/v) 20F and 1500R, capable of amplifying nearly full- glycerol. length 16S rDNA (Weisburg et al. 1991). Sequencing of the housekeeping genes gyrB, rpoD and recA was performed using the primers proposed by Santos & Phenotypic characterization Ochman (2004), Yamamoto & Harayama (1998) and Islam et al. (2013), respectively. PCRs were per- Phenotypic characterization was performed ac- formed basically as indicated in the literature in each cording to Bernardet et al. (1990) and Avendaño- case in a total reaction volume of 25 µl, using the Herrera et al. (2004). The Gram reaction was deter- commercial kit MyTaqTM DNA Polymerase (Bioline) mined according to the KOH method proposed by which includes all necessary reagents except the Buck (1982) and by the Gram-staining method. primers and DNA. PCR products were purified with Temperature tolerance was tested by checking the commercial kit Illustra ExoProStar 1-step (GE growth on Marine Agar (Difco) at 4, 15, 25, 30, 35, Healthcare) following the manufacturer’s instruc- 40 and 45°C for 10 d, and tolerance of salinity was tions. Direct sequencing of purified PCR products tested with growth on basal medium (neopeptone was performed by Secugen (Madrid). The sequences 4g l−1; yeast extract 1 g l−1; agar 15 g l−1) supple- were analyzed using Chromas LITE and BioEdit pro- mented with 0, 3, 6, 8, 10 and 12% (w/v) NaCl. grams and subjected to BLAST (https://blast.ncbi. Growth on thiosulfate–citrate–bile salts–sucrose nlm.nih.gov) and Ez Taxon (www.ezbiocloud.net/ (TCBS) agar (Difco) was also tested. All tests were eztaxon) searches to retrieve the most closely related incubated aerobically at 20°C. Commercial minia- sequences. Se quence similarities were calculated turized API 20E and API 20NE galleries (bio- using SIAS software (http://imed.med.ucm.es/Tools/ Merieux), and Biolog GN2 Micro-plates were also sias). DNA sequences were aligned with others from utilized according to the manufacturer’s instruc- related species using Clustal Omega software, and tions, but sterile sea water was used as a diluent phylogenetic trees were constructed according to and 20°C as the incubation temperature. The type the neighbor-joining method (Saitou & Nei 1987) by strain of Aliivibrio fischeri (CECT 524T) was charac- using the program MEGA. The accuracy of the terized together with the isolates under study, with resulting tree was measured by bootstrap resampling the same methodology. of 1000 replicates. Analysis of fatty acid methyl esters Identification by PCR Preparation of fatty acid methyl esters (FAMEs) A PCR assay using a pair of specific primers target- from strain a591, grown at 20°C on Marine Agar ing the luxA gene of A. fischeri was carried out as plates, was performed according to the instructions previously described (Buller 2004), but using a of the Microbial Identification System (MIDI) as higher annealing temperature (60°C). Template described by Sasser (1990). FAMEs were analyzed by DNA was extracted as mentioned previously and gas chromatography in an Agilent 6850 system, 100 ng of DNA were used for each strain. PCRs were López et al.: Aliivibrio fischeri in diseased brill 217 performed using the commercial kit MyTaqTM DNA length. After recovery by centrifugation (16 168 × g, Polymerase. DNA from the A. fischeri type strain was 2 min), bacteria were washed in phosphate buffered included as a positive control and distilled water as saline (PBS) and finally re-suspended in PBS. Doses negative control. PCR products were electropho- were confirmed with total viable counts after spread- resed on a 2% agarose Tris-borate-EDTA buffer gel ing 0.1 ml volumes of each dose over the surface of stained with SYBR Safe DNA Gel Stain (Invitrogen). duplicate plates of FMM. A control group (chal- A 100 bp DNA ladder H3RTU (Nippon Genetics) was lenged with PBS only) of 10 fish was included in each included as a molecular weight marker. virulence assay. After bacterial challenge, experi- mental and control fish were kept without feeding in 18 l tanks at 18 to 20°C in continually flowing seawa- Molecular fingerprinting ter, and mortalities were recorded daily for a 10 d period. Dead fish were removed and subjected to Template DNA was extracted as mentioned pre - bacteriological examination as previously indicated; viously and 100 ng of DNA were used for each recovered strains were identified by specific PCR. strain. Repetitive extragenic palindromic (REP)-PCR and enterobacteria repetitive intergenic consensus (ERIC) -PCR analysis were performed as previously RESULTS described (Rodríguez et al. 2006) using the commer- cial kit MyTaqTM DNA Polymerase, in a Veriti 96 well Bacterial isolation thermal cycler (Applied Biosystems). PCR products were electrophoresed as mentioned above. Similarity During July 2013, a epizootic outbreak with a high between isolates and the A. fischeri type strain was mortality rate (near 100%) occurred in a marine farm estimated using the Dice similarity coefficient (SD) located in southwestern Spain, affecting brill Scoph- (Dice 1945) with the software DendroUPGMA thalmus rhombus adult cultures in water tempera- (http://genomes.urv.cat/UPGMA). tures of 18 to 20°C. Affected fish showed no external signs of disease. Internally, however, plentiful haem- orrhages were observed, mainly in the liver (Fig. 1). DNA−DNA hybridization Numerous pale yellow colonies appeared in the cul- ture medium from liver and kidney samples, almost For DNA−DNA hybridization assays, DNA was in pure culture. Three isolates (a589, a590 and a591) extracted with the kit NucleoSpin Tissue (Macherey- were selected for identification.
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